Noninvasive Continuous Monitoring of the Effects of Head Position on
Brain Hemodynamics in Ventilated Infants
Adelina Pellicer, MD*; Francisco Gaya´, EE*‡; Rosario Madero, MD*‡; Jose´ Quero, MD*; and Fernando Caban˜as, MD*
ABSTRACT. Hypothesis. Laying supine with the
head in midline position improves cerebral venous re-turn by preventing functional occlusion of the vessels of the neck.
Objectives. To assess changes in cerebral blood vol-ume (⌬CBV) and cerebral blood flow (CBF) with the position of the head in ventilated patients using a non-invasive method. The influence of the type of ventilation and birth weight was evaluated.
Methods. Thirteen conventionally ventilated and 8 high-frequency oscillatory ventilated infants, with mean gestational ages and birth weights of 31 ⴞ 5 weeks (24 –38) and 1575 ⴞ803 g (560 –3000), respectively, were studied 5.8ⴞ7.8 days (1–33) after birth.⌬CBV (mL/100 g) and CBF (mL/100 g/min) were measured by near-infrared spectroscopy with the head in supine midline position (⌬CBVs, CBFs) and rotated 90° to one side (⌬CBVlat, CBFlat). Heart rate, peripheral saturation, transcutaneous PCO2, and blood pressure were monitored continuously. Ventilatory settings remained constant throughout the study period.
Results. Mean⌬CBVs was lower than mean⌬CBVlat, although no changes in blood pressure, transcutaneous PCO2, oxygenation, or heart rate occurred. This change in ⌬CBV was not associated with the type of ventilation or birth weight, but the differences tended to be greater (d⌬CBV ⴝ ⌬CBVlatⴚ⌬CBVs) in the smallest infants (<1200 g). In contrast, CBF did not vary.
Conclusion. The supine midline position of the head favors cerebral venous drainage and helps to prevent elevation of CBV.
Speculation. This finding may be important in the first days of life, particularly in tiny preterm infants recovering from lung disease with improving lung com-pliance, in which functional obstruction of cerebral ve-nous drainage should be avoided. Pediatrics 2002;109: 434 – 440; neonate, cerebral blood volume, cerebral blood flow, head position, mechanical ventilation, near-infrared spectroscopy.
ABBREVIATIONS. CBF, cerebral blood flow; CBV, cerebral blood volume;⌬CBV, changes in cerebral blood volume; SaO2, arterial
oxygen saturation; NIRS, near-infrared spectroscopy; O2Hb,
oxy-hemoglobin; HHb, deoxyoxy-hemoglobin;⌬THb, changes in total he-moglobin;⌬CBVlat, changes in cerebral blood volume with the
head rotated 90° to one side;⌬CBVs, changes in cerebral blood volume with the head in supine midline position; d⌬CBV, differ-ence in cerebral blood volume changes with the head rotated 90° to the side as compared with the midline position.
L
ung mechanics may influence systemic and ce-rebral hemodynamics.1– 6 During intermittent positive-pressure ventilation, air is forced un-der pressure into the lungs, thus increasing pleural pressure and impeding venous return.1The degree to which this occurs, and the attending effects on cardiac output, depends on how much pressure is transmitted to the pleural space and mediastinum, which in turn depends on lung compliance.2 Consid-ering other modalities of mechanical ventilation, an-imal studies of cardiac output during high-frequency oscillation have shown that avoiding lung hyperin-flation prevented a fall in cardiac output.3Concern about the effect of lung mechanics on systemic he-modynamics led the investigation of the effects of mechanical ventilation on brain hemodynamics. Changes in cranial blood volume4and cerebral blood flow (CBF) velocity5 have been found during inter-mittent positive-pressure ventilation. More recently, in a study comparing patients on conventional me-chanical ventilation with patients on high-frequency oscillatory ventilation, no differences were found in CBF velocity, despite lower left cardiac output in the latter.6Given the theoretical effect of ventilatory patterns on brain hemodynamics, particularly when patients are recovering from lung disease, additional func-tional obstruction of cerebral venous drainage might be avoided. Thus, among the factors that have been related with the development and/or extension of intracranial hemorrhage in premature infants, all sit-uations associated with interference with cranial ve-nous drainage, such as raised intrathoracic pressure, large swings in intrathoracic pressure, or raised ve-nous pressure, must be taken into account.7
Postural changes disturb intracranial pressure and CBF velocity in neonates.8,9 Jugular phlebograms10 have shown that rotating the head 90° to one side results in torsion and compression of the internal jugular vein on the same side.
Despite these data, there is no recommendation regarding the optimal head position for ventilated newborn patients.
The aim of our study was to assess by means of a noninvasive method quantitative changes in cerebral From the *Department of Neonatology and ‡Research Unit, La Paz
Univer-sity Hospital, Madrid, Spain.
This work was presented, in part, at the European Society for Pediatric Research Annual Meeting; September 23–27, 2000; Rhodes, Greece. Received for publication Feb 5, 2001; accepted Jul 2, 2001.
Reprint requests to (A.P.) Department of Neonatology, La Paz University Hospital, Paseo de la Castellana, 261, E-28046 Madrid, Spain. E-mail: apellicer@hulp.insalud.es
blood volume (⌬CBV) and CBF according to the position of the head in ventilated patients. The hy-pothesis was that functional occlusion (compression-torsion) of one of the jugular veins obstructs venous drainage and increases CBV. The possible effects of type of ventilation and birth weight also were eval-uated.
METHODS
Twenty-one mechanically ventilated infants admitted to the neonatal intensive care unit at the La Paz University Hospital were studied. Written informed parental consent, approved by the Hu-man Studies Committee, was obtained for all infants before entry in the study.
The studies were performed at least 2 hours after treatment with surfactant or medication likely to affect cerebral circulation. The oxygenation, ventilation, and hemodynamic condition of the patients was stable, thus the dose of medication given in contin-uous perfusion such as sedatives (fentanyl, midazolam, or vecu-ronium) or inotropic drugs (dopamine or dobutamine) remained unvaried during the study period. The optimal position of the endotracheal tube was confirmed by clinical and radiographic criteria. For the⬎1 hour that each study period lasted, patients remained undisturbed in the same position. Tracheal aspiration was conducted 1 hour before and then after the end of the study, depending on individual demands.
Patients were monitored continuously for heart rate, breathing rate, and transcutaneous Pco2. Arterial oxygen saturation (SaO2)
was measured on every pulse beat by pulse oximetry (Fas Trac, Critikon, Sensormedics Corporation, Anaheim, CA). Blood pres-sure was meapres-sured by oscillometry (Dynamap, Critikon). Total hemoglobin concentration (Coulter counter) and serum glucose level were determined at the time of the study.
Near-infrared Spectroscopy (NIRS) Studies
This technique is based on continuous spectrophotometric mea-surement of oxygen-dependent changes in the absorption proper-ties of hemoglobin in the near-infrared range.11With the
assump-tion of a modificaassump-tion of the Beer-Lambert law, changes in hemoglobin concentration can be obtained from changes in light absorption.12,13The sum of the changes in oxyhemoglobin (O
2Hb)
and deoxyhemoglobin (HHb) indicates the changes in total hemo-globin concentration (⌬THb).
The NIRS equipment used was the commercial prototype Critikon Cerebral ReDOX Monitor, with a sensor head containing a photodiode separated 3.5 cm from a light detector. The sensor is connected to the monitor with an electro-optic cable that contains electrical wires and a flexible fiber-optic core consisting of a bun-dle of individual glass fibers. Light pulses from a laser in the monitor are transmitted through the fiber bundle to the sensor head (emission window). Light pulses emerging from the tissue are detected by a single photodiode housed in the sensor head. The signals from the sensor head are carried to the monitor by a shielded pair of electrical cores within the electro-optic cable. The laser diodes produce sequential pulses of monochromatic light, maintaining a precise spectral performance at 4 factory-calibrated wavelengths. A detailed description of the equipment can be found elsewhere.14,15Changes in O
2Hb and HHb concentrations
were calculated from changes in light absorption at each of these wavelengths and are given in micromolar units. A fixed path-length factor of 4.4 was used to correct the pathpath-length of the light for the degree of scattering in brain tissue.16
The sensor was placed frontally on the midline of the forehead
and attached firmly to the skull with stretch bandages in all patients to prevent displacement of the sensor head with modifi-cations of the head.
⌬CBV can be continuously estimated at the bedside by NIRS, because ⌬THb (mol/L) is proportional to⌬CBV (mL/100 g), using the equation17:
⌬CBV⫽K1䡠⌬THb/H
where the value of the constant K1is obtained from the molecular
weight of hemoglobin (64 500), brain tissue density (1.05 g/mL), the large-vessel: tissue ratio, which is assumed to be equal to 0.69,18and decimal conversions. H is the hemoglobin
concentra-tion in a large-vessel blood sample. In the present study, baseline THb was related to an arbitrary zero.⌬THb was calculated as the average value of all the samples obtained in the 20-second period at each measurement time point defined in the study protocol. Therefore,⌬CBV are relative changes from the baseline value.
CBF was measured according to the Fick principle using O2Hb
as an intravascular tracer.19A sudden small change in O 2Hb was
induced by giving the patient a higher inspired fraction of oxygen for several breaths, which caused SaO2to rise rapidly. CBF was
calculated from changes in both parameters recorded over a 6- to 8-second period:
CBF⫽K2䡠(O2Hb-HHb)/2䡠H-integral[O3t] of⌬SaO2
where K2is a constant reflecting the molecular weight of
hemo-globin and cerebral tissue density,20,21 and H was defined as
above.
Study Protocol
Patients lay supine, with the head of the bed tilted 30° upward. The initial position of the head was either midline position or turned 90° to the right or to the left side. After a period of stabilization, ⌬CBV and CBF measurements were performed at intervals of 10 minutes for a 30-minute period, allowing a recovery time between measurements of at least 5 minutes. After this, the position of the head was rotated to 1 side for those patients who started the study with the head in a midline position, and vice versa. After a 5- to 10-minute period of stabilization,⌬CBV and CBF measurements were repeated as described. Figure 1 illus-trates the measurement time points and the intervention.
After every NIRS study, a complete cerebral ultrasound scan was performed to detect changes in parenchymal echogenicity or periventricular-intraventricular hemorrhage. All cerebral ultra-sound studies were made by the same investigator (F.C.).
All NIRS data, as well as SaO2, heart rate, blood pressure, and
Pco2, were recorded simultaneously and stored on a magnetic
disk for later analysis. The same investigator (A.P.) performed all NIRS studies. Analysis of the NIRS curves, including the quality check of raw data and rejection of measurements or calculations, were made off-line using a custom-made computer program.14
CBF calculations were rejected if they did not meet accepted predetermined criteria, considering the stability of (O2Hb-HHb)
and SaO2 before and the stability of THb during the induced
change in oxygenation, the integration time, and the delay be-tween the sudden change in (O2Hb-HHb) and the change in SaO2,
following a published algorithm.22
Statistical Analysis
Data were analyzed using the SPSS9.0 program (SPSS Inc, Chicago, IL).The mean values of⌬CBV, including both positive and negative values, and mean CBF obtained in either position at the 3 measurement time points defined in the study protocol were
Fig 1. Diagram illustrating the study protocol. The continuous line repre-sents⌬THb (mol/L) with respect to baseline, related to an arbitrary zero. The measurement time points at each position of the head (T1,2,3, and T⬘1,2,3)
calculated for each individual. Quantitative data are given as means (SEM). To study the effect of changing the position of the head on the different variables, a paired ttest or the Wilcoxon signed-rank test was used, depending on data distribution. Fur-thermore, to explore the effect of changing the position of the head on⌬CBV, a 2-way analysis of variance for repeated measurements was performed, factoring for head position (supine midline or rotated 90° to the side) and time (T1, T2, T3,or T⬘1, T⬘2, T⬘3). First,
we studied the main effects of each factor; that is, the behavior of the average values obtained at each position or the average value for position at each time. In addition, the mean linear trend in time was analyzed. Interaction between factors was included. To study the relationship between positional changes in⌬CBV and CBF and changes in other variables, such as mean blood pressure, heart rate, Pco2, birth weight, or gestational age, we used the Spearman
correlation coefficient. Postural changes in brain hemodynamics (⌬CBV and CBF) in patients grouped by birth weight (under or over 1200 g) and type of mechanical ventilation (synchronized intermittent mandatory ventilation or high-frequency oscillatory ventilation), were analyzed using covariance analysis. The covari-ants considered were heart rate, mean blood pressure, and Pco2.
All statistical analyses were considered bilateral.P values⬍.05 were considered significant.
RESULTS
The 21 neonates studied had a mean gestational age and birth weight of 30.9⫾4.9 weeks (24 –38) and 1575 ⫾ 803 g (560 –3000), respectively. The mean postnatal age of patients at the time of the study was 5.8 ⫾ 7.8 days, but 47.6% of the studies were done within the first 72 hours of life, and 90% of the studies were done in the first week of life. Among the patients, 13 were on synchronized intermittent man-datory ventilation and the remaining 8 were on high-frequency oscillation. Relevant clinical data are shown in Table 1.
Regarding NIRS studies, CBF measurements were unsuccessful in 9 infants because a suitable change in SaO2could not be induced in infants receiving a high inspired oxygen fraction. Consequently, CBF data were obtained from 12 patients (cases 1–5, 8, 12, 15–18, and 20). In these patients, satisfactory re-sponses to the inspired oxygen fraction changes were obtained, allowing us to measure CBF at least 3 times in each position, from which the mean values were calculated.
Table 2 shows the mean values of⌬CBV, CBF, and physiologic variables (heart rate, blood pressure, and Pco2) with respect to the position of the head. Serum glucose level was within normal ranges in all infants. The mean ⌬CBV was significantly higher when the head was rotated 90° to the side than when the head was in midline position. The individual mean⌬CBV resulting from changing the position of the head are shown in Fig 2. In contrast, no significant changes were observed in mean CBF values or any physio-logic variable. Ventilatory settings remained un-changed during the study period. No correlation was found between changes in ⌬CBV and changes in CBF, heart rate, mean blood pressure, or Pco2.
In addition, the effect of head position on⌬CBV at the different measurement time points is illustrated in Fig 3. The analysis of variance for repeated mea-surements shows a significant increase in ⌬CBV when the head was rotated 90° to the side as com-pared with midline position (P⫽ .026). Also, a sig-nificant linear increase in ⌬CBV in relation to time was observed (P ⬍.01; Fig 3).
The type of mechanical ventilation did not affect the postural changes in the CBV of our patients. Figure 4 shows the difference in⌬CBV with the head rotated 90° to the side with respect to midline posi-tion (d⌬CBV⫽ ⌬CBVlat⫺⌬CBVs) in patients on syn-chronized intermittent mandatory ventilation and on high-frequency oscillation.
In our study, no relationship was found between postural ⌬CBV changes and birth weight or gesta-tional age. Although there was a trend toward higher d⌬CBV values in the smallest patients (ⱕ1200 g) as compared with heavier ones (⬎1200 g), the differ-ences did not reach statistical significance (Fig 5).
DISCUSSION
In the present study, we investigated the changes in⌬CBV and CBF that occur in relation to the posi-tion of the head. We examined only 2 posiposi-tions (su-pine midline and su(su-pine-90° rotation) because our study was made in mechanically ventilated patients, who usually lie supine, particularly during the first days of life when umbilical catheters are often in place. Also, to facilitate chest movements in venti-lated patients we keep the head of the mattress tilted 30° upward. However, rotation of the head is routine in the normal handling of these infants for, among other reasons, postural changes, aspiration of the endotracheal tube, or surfactant instillation.
In adult neurosurgery and intensive care patients, maintaining the head in the midline position and elevating the head of the bed 30° have been recog-nized clinically to reduce cerebral venous pressure and intracranial pressure by promoting hydrostatic cerebral venous drainage.24Studies in neonates have yielded discrepant results. Although some studies show that, at lower levels of intracranial pressure, elevation of the head 30° does not significantly lower intracranial pressure as compared with the horizon-tal position,25 others8find a significant reduction in intracranial pressure at any baseline pressure level. However, in the 2 studies cited8,25tilting the head 30° up significantly lowered intracranial pressure when intracranial pressure was above certain limits. The limitation of intracranial compliance would explain these facts. Thus, at higher levels of intracranial pres-sure, any change in venous pressure will be associ-ated with more marked changes in intracranial pres-sure.
On the other hand, there is an arterial pressure difference between the head and right arm with 30° elevation of the head.26In the present study, the head was kept elevated throughout the study period, so further effects on cerebral venous drainage and cra-nial arterial pressure were avoided.
ligation or thrombus formation, cerebral venous re-turn may be greatly compromised. Newborn studies of blood flow velocity in the superior sagittal sinus have shown great variability in cranial venous drain-age in the resting state.27In fact, at one extreme are infants dependent on a single jugular vein and at the other are infants using both jugular veins and the vertebral veins as well. There is usually a dominant
side, that is, the side on which most drainage occurs. Nonjugular paths may be in use all the time, or become functional when major venous pathways are obstructed.27 These findings probably explain the wide range of responses in CBV to rotation of the head observed in this study (Fig 2).
The mean change in blood volume with rotation of the head (⌬CBVlat⫺⌬CBVs) in this study was nearly 0.74 mL/100 g. Assuming that reference absolute values of CBV in neonates, calculated by NIRS, are 2 to 3 mL/100 g,14,28,29this sustained change in⌬CBV would represent a 24.6% to 37% increase in CBV. The rate of change in CBV is also noteworthy. The first measurement time point was after a 5 to 10 minutes period of stabilization after the intervention. The
Fig 2. Individual postural variation in CBV. The individual mean
⌬CBV in supine midline position and with the head rotated 90° to the side is shown.
Fig 3. Effect of head position on CBV. The mean values of CBV changes at each measurement time point in supine midline posi-tion (dotted line) and with the head rotated 90° to the side (con-tinuous line) are shown. The analysis of variance for repeated measurements shows a significant increase in⌬CBVlat as com-pared with⌬CBVs (P⫽.026). Also, a significant linear increase in
⌬CBV in relation to time was observed (P⬍.01).
Fig 4. Postural variation in CBV in relation to type of mechanical ventilation. The difference in⌬CBV with the head rotated 90° to the side as compared with the midline position (d⌬CBV ⫽ ⌬CBVlat⫺⌬CBVs) in patients on synchronized intermittent man-datory ventilation (SIMV) or high-frequency oscillation (HFO) are shown.
Fig 5. Postural variation in CBV in patients grouped by birth weight. The difference in ⌬CBV with the head rotated 90° to the side as compared with midline position (d⌬CBV ⫽
⌬CBVlat⫺⌬CBV) in patientsⱕ1200 g birth weight and patients
⬎1200 g birth weight are shown. TABLE 2. Mean (SEM) Values of⌬CBV, CBF, and
Physiolog-ical Variables According to the Position of the Head Supine,
Midline
Supine, Turned 90° Right/Left
P
Value
⌬CBV (mL/100 g) 0.002 (0.2) 0.74 (0.2) ⬍.05* CBF (mL/100 g/min) 37.6 (3.7) 33.7 (3.4)
Mean blood pressure (mm Hg)
48 mm Hg (2) 48 mm Hg (2)
Heart rate 141 (4) 143 (3) Pco2(mm Hg) 54 (3) 50 (2)
changes in CBV observed in relation to the position of the head are rapid and sustained, as is clearly illustrated in Fig 3. Although the cause of intracranial hemorrhage seems to be multifactorial, subependy-mal vessels have been shown to be vulnerable to changes in venous pressure and blood volume in experimental studies,30especially if there has been a preceding period of asphyxia. Given the distensibil-ity of the neonatal skull, variations in vascular trans-mural pressure may occur with the changes in blood volume; this effect will be larger with smaller in-creases in intracranial pressure in the case of highly compliant skulls. Obstruction of venous return by an unfavorable head position thus may expose the infant to increased venous volume and pressure, and increase the risk of intracranial bleeding. Al-though we have not found a correlation between postural changes in ⌬CBV and birth weight, the (⌬CBVlat⫺CBV) changes seemed to be higher in the smallest patients (Fig 4). This may be attributed to their more compliant neck structures, but they also would have more compliant skulls. Changes in ve-nous transmural pressure may be broader in range and the risk of intracranial bleeding could be greater. In our study, there were no simultaneous varia-tions in SaO231or Pco2,17,32that could have affected CBV independently. These facts further support pos-tural functional obstruction of venous drainage with rotation of the head.
The cerebral hemodynamic changes observed in this study did not indicate any repercussion on CBF. No changes in mean arterial pressure occurred with postural changes in our study so one must assume that no changes in intracranial mean arterial pressure took place because the elevation of the head was the same for all postures.26As discussed before, changes in intracranial pressure with CBV changes should not be important in the case of very compliant skulls, thus changes in cerebral perfusion pressure and CBF should not be expected. On the other hand, autor-regulatory mechanisms operate quickly in hu-mans33,34to maintain a constant CBF. Dynamic cere-bral autorregulation, although absent in high-risk preterm infants, is intact in neurologically healthy term infants.35Most of the 12 patients in which CBF measurements were performed were ⬎1900 g and had no major neurologic problems (Table 1). We therefore assume that cerebral autorregulatory mechanisms were functional in this population.
The pattern of ventilation may alter brain hemo-dynamics,4 – 6,36particularly when lung compliance is high and positive and negative pressures can be transmitted more effectively to intrathoracic struc-tures.4 Although the studies are not comparable, negative end-expiratory pressure apparently favors cerebral venous return and lowers CBV,36 as does spontaneous inspiration.4 In contrast, intermittent positive-pressure ventilation, particularly when pressure changes are effectively transmitted,4,5 in-creases CBV4and causes fluctuations in cerebral ve-nous flow velocity.5 In 1 study,36 switching from intermittent positive-pressure ventilation with posi-tive end-expiratory pressure to endotracheal contin-uous positive airway pressure reduced CBV. The
introduction of new modalities of mechanical venti-lation, particularly high-frequency oscilventi-lation, actu-ally widely used, raised the question of the effect it might have on systemic and cerebral hemodynamics. However, it has been shown that although patients on high-frequency oscillation have lower left cardiac output than patients on conventional mechanical ventilation, CBF velocity does not differ.6
The combined effect of mechanical ventilation and jugular venous compression on cerebral venous drainage has been explored in neurosurgery. Re-search focusing on the prevention of cerebral venous air embolism when surgical procedures are per-formed in the sitting position with subatmospheric venous blood pressure at the level of the surgical wound, has shown that even very high end-expira-tory pressures do not increase cerebral venous pres-sure, in contrast with jugular venous compres-sion.37,38Nevertheless, these studies were performed on adult animal models37 and children,38 but not neonates, who have significantly more compliant chest, neck and cranial structures.
In the present study, we assumed that there was no change in lung compliance because no changes in blood gases or physiologic variables were detected. The study was too short to detect substantial changes related with pulmonary disease and no acute event significant enough to cause important swings in in-trathoracic pressure occurred. Respiratory settings remained constant. Therefore, we conclude that the effects on CBV observed in this study were related to obstruction of the venous drainage at the level of the neck. Although theoretical differences in lung me-chanics may exist, we did not observe differences in the effects of the 2 modalities of ventilation on cere-bral venous return.
Continuous estimation of ⌬CBV by NIRS at the cotside of patients may be a useful and easy way of identifying the dominant side for cerebral venous drainage, thus allowing us to explore noninvasively the effects of postural changes on CBV. Given the variability of cranial venous drainage,27as supported by the broad range of ⌬CBV changes found in this study, this kind of monitoring could be an important adjunct to the routine handling of sick infants.
ACKNOWLEDGMENTS
This study was supported by a grant from the Fondo de Inves-tigacio´n Sanitaria (FIS 94/0198).
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“ALMOST MEASUREMENTS”
“Whatever we measure [in the real world] is really part of a random scatter, whose probabilities are described by a mathematical function, the distribution function. . . the numbers that identify the distribution function (eg, mean, standard deviation) are not the same type of ‘number’ as the measurements. These numbers can never be observed, but can be inferred from the way in which the measure-ments scatter. These numbers [are] called parameters—from the Greek for ‘almost measurements.’”
Salsburg D.The Lady Tasting Tea: How Statistics Revolutionized Science in the Twentieth Century.New York, NY: WH Freeman; 2001
DOI: 10.1542/peds.109.3.434
2002;109;434
Pediatrics
Adelina Pellicer, Francisco Gayá, Rosario Madero, José Quero and Fernando Cabañas
Hemodynamics in Ventilated Infants
Noninvasive Continuous Monitoring of the Effects of Head Position on Brain
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DOI: 10.1542/peds.109.3.434
2002;109;434
Pediatrics
Adelina Pellicer, Francisco Gayá, Rosario Madero, José Quero and Fernando Cabañas
Hemodynamics in Ventilated Infants
Noninvasive Continuous Monitoring of the Effects of Head Position on Brain
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